Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors.
Germline transposon silencing
Neuronal wiring
Nuclear pore complex
Piwi-interacting RNA (piRNA)
Promoter evolution
RNA transgenerational inheritance
Rapid evolution
Speciation
Transposon silencing
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
08 Jul 2024
08 Jul 2024
Historique:
received:
10
04
2024
accepted:
01
07
2024
medline:
9
7
2024
pubmed:
9
7
2024
entrez:
8
7
2024
Statut:
epublish
Résumé
The piRNA pathway in animal gonads functions as an 'RNA-based immune system', serving to silence transposable elements and prevent inheritance of novel invaders. In Drosophila, this pathway relies on three gonad-specific Argonaute proteins (Argonaute-3, Aubergine and Piwi) that associate with 23-28 nucleotide piRNAs, directing the silencing of transposon-derived transcripts. Transposons constitute a primary driver of genome evolution, yet the evolution of piRNA pathway factors has not received in-depth exploration. Specifically, channel nuclear pore proteins, which impact piRNA processing, exhibit regions of rapid evolution in their promoters. Consequently, the question arises whether such a mode of evolution is a general feature of transposon silencing pathways. By employing genomic analysis of coding and promoter regions within genes that function in transposon silencing in Drosophila, we demonstrate that the promoters of germ cell-specific piRNA factors are undergoing rapid evolution. Our findings indicate that rapid promoter evolution is a common trait among piRNA factors engaged in germline silencing across insect species, potentially contributing to gene expression divergence in closely related taxa. Furthermore, we observe that the promoters of genes exclusively expressed in germ cells generally exhibit rapid evolution, with some divergence in gene expression. Our results suggest that increased germline promoter evolution, in partnership with other factors, could contribute to transposon silencing and evolution of species through differential expression of genes driven by invading transposons.
Sections du résumé
BACKGROUND
BACKGROUND
The piRNA pathway in animal gonads functions as an 'RNA-based immune system', serving to silence transposable elements and prevent inheritance of novel invaders. In Drosophila, this pathway relies on three gonad-specific Argonaute proteins (Argonaute-3, Aubergine and Piwi) that associate with 23-28 nucleotide piRNAs, directing the silencing of transposon-derived transcripts. Transposons constitute a primary driver of genome evolution, yet the evolution of piRNA pathway factors has not received in-depth exploration. Specifically, channel nuclear pore proteins, which impact piRNA processing, exhibit regions of rapid evolution in their promoters. Consequently, the question arises whether such a mode of evolution is a general feature of transposon silencing pathways.
RESULTS
RESULTS
By employing genomic analysis of coding and promoter regions within genes that function in transposon silencing in Drosophila, we demonstrate that the promoters of germ cell-specific piRNA factors are undergoing rapid evolution. Our findings indicate that rapid promoter evolution is a common trait among piRNA factors engaged in germline silencing across insect species, potentially contributing to gene expression divergence in closely related taxa. Furthermore, we observe that the promoters of genes exclusively expressed in germ cells generally exhibit rapid evolution, with some divergence in gene expression.
CONCLUSION
CONCLUSIONS
Our results suggest that increased germline promoter evolution, in partnership with other factors, could contribute to transposon silencing and evolution of species through differential expression of genes driven by invading transposons.
Identifiants
pubmed: 38977960
doi: 10.1186/s12864-024-10584-9
pii: 10.1186/s12864-024-10584-9
doi:
Substances chimiques
DNA Transposable Elements
0
RNA, Small Interfering
0
Drosophila Proteins
0
Argonaute Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
678Informations de copyright
© 2024. The Author(s).
Références
Iwakawa HO, Tomari Y. Life of RISC: Formation, action, and degradation of RNA-induced silencing complex. Mol Cell. 2022;82(1):30–43.
pubmed: 34942118
doi: 10.1016/j.molcel.2021.11.026
Czech B, Munafò M, Ciabrelli F, Eastwood EL, Fabry MH, Kneuss E, Hannon GJ. piRNA-guided genome defense: from biogenesis to silencing. Annu Rev Genet. 2018;52(1):131–57.
pubmed: 30476449
pmcid: 10784713
doi: 10.1146/annurev-genet-120417-031441
Yamashiro H, Siomi MC. PIWI-interacting RNA in Drosophila: biogenesis, transposon regulation, and beyond. Chem Rev. 2018;118(8):4404–21.
pubmed: 29281264
doi: 10.1021/acs.chemrev.7b00393
Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8(4):272–85.
pubmed: 17363976
doi: 10.1038/nrg2072
Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, Hannon GJ. Specialized piRNA pathways act in germline and somatic tissues of the drosophila ovary. Cell. 2009;137(3):522–35.
pubmed: 19395010
pmcid: 2882632
doi: 10.1016/j.cell.2009.03.040
Khurana JS, Theurkauf W. piRNAs, transposon silencing, and Drosophila germline development. J Cell Biol. 2010;191(5):905–13.
pubmed: 21115802
pmcid: 2995163
doi: 10.1083/jcb.201006034
Senti K-A, Brennecke J. The piRNA pathway: a fly’s perspective on the guardian of the genome. Trends Genet. 2010;26(12):499–509.
pubmed: 20934772
pmcid: 4988489
doi: 10.1016/j.tig.2010.08.007
Sakakibara K, Siomi MC. The PIWI-Interacting RNA molecular pathway: insights from cultured silkworm germline cells. BioEssays. 2018;40(1):1700068.
doi: 10.1002/bies.201700068
Moelling K. Epigenetics and transgenerational inheritance. J Physiol. 2024;602(11):2537–45.
pubmed: 37772441
doi: 10.1113/JP284424
Grentzinger T, Armenise C, Brun C, Mugat B, Serrano V, Pelisson A, Chambeyron S. piRNA-mediated transgenerational inheritance of an acquired trait. Genome Res. 2012;22(10):1877–88.
pubmed: 22555593
pmcid: 3460183
doi: 10.1101/gr.136614.111
Wang X, Ramat A, Simonelig M, Liu M-F. Emerging roles and functional mechanisms of PIWI-interacting RNAs. Nat Rev Mol Cell Biol. 2023;24(2):123–41.
pubmed: 36104626
doi: 10.1038/s41580-022-00528-0
Sato K, Siomi MC. The piRNA pathway in Drosophila ovarian germ and somatic cells. Proc Jpn Acad Ser B. 2020;96(1):32–42.
doi: 10.2183/pjab.96.003
Signor S, Vedanayagam J, Kim BY, Wierzbicki F, Kofler R, Lai EC. Rapid evolutionary diversification of the flamenco locus across simulans clade Drosophila species. PLoS Genet. 2023;19(8):e1010914.
pubmed: 37643184
pmcid: 10495008
doi: 10.1371/journal.pgen.1010914
Czech B, Hannon GJ. One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends Biochem Sci. 2016;41(4):324–37.
pubmed: 26810602
pmcid: 4819955
doi: 10.1016/j.tibs.2015.12.008
Haase AD. An introduction to PIWI-interacting RNAs (piRNAs) in the context of metazoan small RNA silencing pathways. RNA Biol. 2022;19(1):1094–102.
pubmed: 36217279
pmcid: 9559041
doi: 10.1080/15476286.2022.2132359
Czech B, Preall JB, McGinn J, Hannon GJ. A transcriptome-wide RNAi screen in the drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell. 2013;50(5):749–61.
pubmed: 23665227
pmcid: 3724427
doi: 10.1016/j.molcel.2013.04.007
Brown JS, Zhang D, Gaylord O, Chen W, Lee HC. Sensitized piRNA reporter identifies multiple RNA processing factors involved in piRNA-mediated gene silencing. Genetics. 2023;224(4):iyad095.
Handler D, Meixner K, Pizka M, Lauss K, Schmied C, Gruber FS, Brennecke J. The genetic makeup of the drosophila piRNA pathway. Mol Cell. 2013;50(5):762–77.
pubmed: 23665231
pmcid: 3679447
doi: 10.1016/j.molcel.2013.04.031
Munafò M, Lawless VR, Passera A, Macmillan S, Bornelöv S, Haussmann IU, Soller M, Hannon GJ, Czech B. Channel nuclear pore complex subunits are required for transposon silencing in Drosophila. eLife. 2021;10:e66321.
pubmed: 33856346
pmcid: 8133776
doi: 10.7554/eLife.66321
Nallasivan MP, Haussmann IU, Civetta A, Soller M. Channel nuclear pore protein 54 directs sexual differentiation and neuronal wiring of female reproductive behaviors in Drosophila. BMC Biol. 2021;19(1):226.
pubmed: 34666772
pmcid: 8527774
doi: 10.1186/s12915-021-01154-6
McQuarrie DWJ, Read AM, Stephens FHS, Civetta A, Soller M. Indel driven rapid evolution of core nuclear pore protein gene promoters. Sci Rep. 2023;13(1):8035.
pubmed: 37198214
pmcid: 10192361
doi: 10.1038/s41598-023-34985-0
Haussmann IU, Hemani Y, Wijesekera T, Dauwalder B, Soller M. Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours. Proc Biol Sci. 2013;280(1771):20131938.
pubmed: 24089336
pmcid: 3790487
Tang S, Presgraves DC. Evolution of the Drosophila nuclear pore complex results in multiple hybrid Incompatibilities. Science. 2009;323(5915):779–82.
pubmed: 19197064
pmcid: 2826207
doi: 10.1126/science.1169123
Tang S, Presgraves DC. Lineage-specific evolution of the complex Nup160 hybrid incompatibility between Drosophila melanogaster and its sister species. Genetics. 2015;200(4):1245–54.
pubmed: 26022241
pmcid: 4574247
doi: 10.1534/genetics.114.167411
Iwasaki YW, Siomi MC, Siomi H. PIWI-interacting RNA: its biogenesis and functions. Annu Rev Biochem. 2015;84:405–33.
pubmed: 25747396
doi: 10.1146/annurev-biochem-060614-034258
Taylor MS, Kai C, Kawai J, Carninci P, Hayashizaki Y, Semple CAM. Heterotachy in Mammalian promoter evolution. PLoS Genet. 2006;2(4):e30.
pubmed: 16683025
pmcid: 1449885
doi: 10.1371/journal.pgen.0020030
Balacco DL, Soller M. The m(6)A writer: rise of a machine for growing tasks. Biochemistry. 2019;58(5):363–78.
pubmed: 30557013
doi: 10.1021/acs.biochem.8b01166
Bawankar P, Lence T, Paolantoni C, Haussmann IU, Kazlauskiene M, Jacob D, Heidelberger JB, Richter FM, Nallasivan MP, Morin V, et al. Hakai is required for stabilization of core components of the m6A mRNA methylation machinery. Nat Commun. 2021;12(1):3778.
pubmed: 34145251
pmcid: 8213727
doi: 10.1038/s41467-021-23892-5
van Lopik J, Alizada A, Trapotsi MA, Hannon GJ, Bornelöv S, Czech Nicholson B. Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across the Drosophila genus. Nat Commun. 2023;14(1):7337.
pubmed: 37957172
pmcid: 10643416
doi: 10.1038/s41467-023-42787-1
Fridrich A, Moran Y. Some flies do not play ping-pong. PLoS Biol. 2023;21(6):e3002152.
pubmed: 37285339
pmcid: 10246807
doi: 10.1371/journal.pbio.3002152
Chary S, Hayashi R. Mechanistic divergence of piRNA biogenesis in Drosophila. bioRxiv. 2022.11.14.516378.
McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991;351(6328):652–4.
pubmed: 1904993
doi: 10.1038/351652a0
Karolchik D. The UCSC table browser data retrieval tool. Nucleic Acids Res. 2004;32(90001):493D – 496.
doi: 10.1093/nar/gkh103
Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. The human genome browser at UCSC. Gen Res. 2002;12(6):996–1006.
doi: 10.1101/gr.229102
Consortium GO. The gene ontology resource: enriching a GOld mine. Nucleic Acids Res. 2021;49(D1):D325-d334.
doi: 10.1093/nar/gkaa1113
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000;25(1):25–9.
pubmed: 10802651
pmcid: 3037419
doi: 10.1038/75556
Mi H, Muruganujan A, Ebert D, Huang X, Thomas PD. PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res. 2018;47(D1):D419–26.
pmcid: 6323939
doi: 10.1093/nar/gky1038
Sanfilippo P, Wen J, Lai EC. Landscape and evolution of tissue-specific alternative polyadenylation across Drosophila species. Gen Biol. 2017;18(1):229.
doi: 10.1186/s13059-017-1358-0
Smolko AE, Shapiro-Kulnane L, Salz HK. The H3K9 methyltransferase SETDB1 maintains female identity in Drosophila germ cells. Nat Commun. 2018;9(1):259473.
doi: 10.1038/s41467-018-06697-x
Vankuren NW, Vibranovski MD. A novel dataset for identifying sex-biased genes in Drosophila. J Genomics. 2014;2:64–7.
pubmed: 25031657
pmcid: 4091448
doi: 10.7150/jgen.7955
Hart CM, Cuvier O, Laemmli UK. Evidence for an antagonistic relationship between the boundary element-associated factor BEAF and the transcription factor DREF. Chromosoma. 1999;108(6):375–83.
pubmed: 10591997
doi: 10.1007/s004120050389
Yang J, Ramos E, Corces VG. The BEAF-32 insulator coordinates genome organization and function during the evolution of Drosophila species. Genome Res. 2012;22(11):2199–207.
pubmed: 22895281
pmcid: 3483549
doi: 10.1101/gr.142125.112
Sawado T, Hirose F, Takahashi Y, Sasaki T, Shinomiya T, Sakaguchi K, Matsukage A, Yamaguchi M. The DNA replication-related element (DRE)/DRE-binding factor system is a transcriptional regulator of the Drosophila E2FGene*. J Biol Chem. 1998;273(40):26042–51.
pubmed: 9748283
doi: 10.1074/jbc.273.40.26042
Kim J, Johnson K, Chen HJ, Carroll S, Laughon A. Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature. 1997;388(6639):304–8.
pubmed: 9230443
doi: 10.1038/40906
Alizada A, Hannon GJ, Nicholson BC. Ovo is a master regulator of the piRNA pathway in animal ovarian germ cells. bioRxiv. 2024.04.23.590802.
Eastwood EL, Jara KA, Bornelöv S, Munafò M, Frantzis V, Kneuss E, Barbar EJ, Czech B, Hannon GJ. Dimerisation of the PICTS complex via LC8/Cut-up drives co-transcriptional transposon silencing in Drosophila. eLife. 2021;10:e65557.
pubmed: 33538693
pmcid: 7861614
doi: 10.7554/eLife.65557
Treiber CD, Waddell S. Transposon expression in the Drosophila brain is driven by neighboring genes and diversifies the neural transcriptome. Genome Res. 2020;30(11):1559–69.
pubmed: 32973040
pmcid: 7605248
doi: 10.1101/gr.259200.119
Laverty C, Lucci J, Akhtar A. The MSL complex: X chromosome and beyond. Curr Opin Genet Dev. 2010;20(2):171–8.
pubmed: 20167472
doi: 10.1016/j.gde.2010.01.007
Straub T, Becker PB. Dosage compensation: the beginning and end of generalization. Nat Rev Genet. 2007;8(1):47–57.
pubmed: 17173057
doi: 10.1038/nrg2013
Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science. 2008;322(5906):1387–92.
pubmed: 19039138
pmcid: 2805124
doi: 10.1126/science.1165171
Luo Y, He P, Kanrar N, Fejes Toth K, Aravin AA. Maternally inherited siRNAs initiate piRNA cluster formation. Mol Cell. 2023;83:3835–51.
pubmed: 37875112
doi: 10.1016/j.molcel.2023.09.033
Parhad SS, Yu T, Zhang G, Rice NP, Weng Z, Theurkauf WE. Adaptive evolution targets a piRNA precursor transcription network. Cell Rep. 2020;30(8):2672-2685.e2675.
pubmed: 32101744
pmcid: 7061269
doi: 10.1016/j.celrep.2020.01.109
Parhad SS, Tu S, Weng Z, Theurkauf WE. Adaptive evolution leads to cross-species incompatibility in the piRNA transposon silencing machinery. Dev Cell. 2017;43(1):60-70.e65.
pubmed: 28919205
pmcid: 5653967
doi: 10.1016/j.devcel.2017.08.012
Kelleher ES, Edelman NB, Barbash DA. Drosophila interspecific hybrids phenocopy piRNA-pathway mutants. PLoS Biol. 2012;10(11):e1001428.
pubmed: 23189033
pmcid: 3506263
doi: 10.1371/journal.pbio.1001428
Vermaak D, Henikoff S, Malik HS. Positive selection drives the evolution of rhino, a member of the heterochromatin protein 1 family in drosophila. PLoS Genet. 2005;1(1):e9.
pubmed: 16103923
pmcid: 1183528
doi: 10.1371/journal.pgen.0010009
Obbard DJ, Finnegan DJ. RNA interference: endogenous siRNAs derived from transposable elements. Curr Biol. 2008;18(13):R561–3.
pubmed: 18606126
doi: 10.1016/j.cub.2008.05.035
Blumenstiel JP, Erwin AA, Hemmer LW. What drives positive selection in the drosophila piRNA machinery? The genomic autoimmunity hypothesis. Yale J Biol Med. 2016;89(4):499–512.
pubmed: 28018141
pmcid: 5168828
Wang L, Barbash DA, Kelleher ES. Adaptive evolution among cytoplasmic piRNA proteins leads to decreased genomic auto-immunity. PLoS Genet. 2020;16(6):e1008861.
pubmed: 32525870
pmcid: 7310878
doi: 10.1371/journal.pgen.1008861
Parhad SS, Theurkauf WE. Rapid evolution and conserved function of the piRNA pathway. Open Biol. 2019;9(1):180181.
pubmed: 30958115
doi: 10.1098/rsob.180181
Lawlor MA, Ellison CE. Evolutionary dynamics between transposable elements and their host genomes: mechanisms of suppression and escape. Curr Opin Genet Dev. 2023;82:102092.
pubmed: 37517354
doi: 10.1016/j.gde.2023.102092
Soller M, Haussmann IU, Hollmann M, Choffat Y, White K, Kubli E, Schäfer MA. Sex-peptide-regulated female sexual behavior requires a subset of ascending ventral nerve cord neurons. Curr Biol. 2006;16(18):1771–82.
pubmed: 16979554
doi: 10.1016/j.cub.2006.07.055
Fan Y, Soller M, Flister S, Hollmann M, Müller M, Bello B, Egger B, White K, Schäfer MA, Reichert H. The egghead gene is required for compartmentalization in Drosophila optic lobe development. Dev Biol. 2005;287(1):61–73.
pubmed: 16182276
doi: 10.1016/j.ydbio.2005.08.031
Seeholzer LF, Seppo M, Stern DL, Ruta V. Evolution of a central neural circuit underlies Drosophila mate preferences. Nature. 2018;559(7715):564–9.
pubmed: 29995860
pmcid: 6276375
doi: 10.1038/s41586-018-0322-9
Main BJ, Smith AD, Jang H, Nuzhdin SV. Transcription start site evolution in Drosophila. Mol Biol Evol. 2013;30(8):1966–74.
pubmed: 23649539
pmcid: 3708499
doi: 10.1093/molbev/mst085
Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38(7):3022–7.
pubmed: 33892491
pmcid: 8233496
doi: 10.1093/molbev/msab120
Lack JB, Cardeno CM, Crepeau MW, Taylor W, Corbett-Detig RB, Stevens KA, Langley CH, Pool JE. The Drosophila genome nexus: a population genomic resource of 623 Drosophila melanogaster genomes, including 197 from a single ancestral range population. Genetics. 2015;199(4):1229–41.
pubmed: 25631317
pmcid: 4391556
doi: 10.1534/genetics.115.174664
Lack JB, Lange JD, Tang AD, Corbett-Detig RB, Pool JE. A thousand fly genomes: an expanded Drosophila genome nexus. Mol Biol Evol. 2016;33(12):3308–13.
pubmed: 27687565
pmcid: 5100052
doi: 10.1093/molbev/msw195
Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, et al. The Drosophila melanogaster genetic reference panel. Nature. 2012;482(7384):173–8.
pubmed: 22318601
pmcid: 3683990
doi: 10.1038/nature10811
Gramates LS, Agapite J, Attrill H, Calvi BR, Crosby MA, dos Santos G, Goodman JL, Goutte-Gattat D, Jenkins VK, Kaufman T, et al. FlyBase: a guided tour of highlighted features. Genetics. 2022;220(4):iyac035.
pubmed: 35266522
pmcid: 8982030
doi: 10.1093/genetics/iyac035
Tang H, Lewontin RC. Locating regions of differential variability in DNA and protein sequences. Genetics. 1999;153(1):485–95.
pubmed: 10471728
pmcid: 1460758
doi: 10.1093/genetics/153.1.485
Bailey TL, Grant CE. SEA: simple enrichment analysis of motifs. bioRxiv. 2021.08.23.457422.
Bailey TL, Johnson J, Grant CE, Noble WS. The MEME suite. Nucleic Acids Res. 2015;43(W1):W39-49.
pubmed: 25953851
pmcid: 4489269
doi: 10.1093/nar/gkv416
Yanai I, Benjamin H, Shmoish M, Chalifa-Caspi V, Shklar M, Ophir R, Bar-Even A, Horn-Saban S, Safran M, Domany E, et al. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics. 2004;21(5):650–9.
pubmed: 15388519
doi: 10.1093/bioinformatics/bti042
Leader DP, Krause SA, Pandit A, Davies SA, Dow JAT. FlyAtlas 2: a new version of the Drosophila melanogaster expression atlas with RNA-Seq, miRNA-Seq and sex-specific data. Nucleic Acids Res. 2017;46(D1):D809–15.
pmcid: 5753349
doi: 10.1093/nar/gkx976